Stand Alone Conference of the American Society of Naturalists

Symposium I: Maladaptive Evolution

Saturday, 6 January 2018, 1:00-5:30 PM

Throughout the history of evolutionary biology, scientists have marveled at adaptation and trained their sights on the ways that natural selection shapes the evolution of fitness advantages. Indeed, the terms adaptation and evolution have become nearly synonymous. By contrast, the processes and occurrences of maladaptation (the evolution of relative and absolute fitness declines) have received less attention. This relative lack of inquiry into maladaptation is surprising when we consider that the overwhelming majority of species that have ever existed are now extinct, making clear the inescapable and pervasive nature of maladaptation. Indeed, literature reviews indicate that even in contexts where local adaptation is expected, maladaptation is present in about 1/3 of the cases. Maladaptation, it seems, is as much a product of evolutionary dynamics as is adaptation.

Despite the apparent prevalence of maladaptive evolution, we understand very little about its dynamics and distribution. For example, each year the number of papers concerning adaptive evolution exceeds that of maladaptive evolution by an order of magnitude. Importantly, the few studies formally emphasizing and studying maladaptation have received only modest attention, perhaps because their fragmented and scattered appearance in the literature makes them seem like exceptions to the general rule of strong adaptation.

We hope that this symposium will pave the way to a more balanced study of evolution by catalyzing the development of insights into the phenomenon of maladaptation. By showing that maladaptation is actually common and potentially increasing—and by providing a clear approach for studying and communicating maladaptation—we hope to foster the development of a more balanced study of evolution, one that accurately characterizes both adaptive and maladaptive fitness dynamics.

Symposium Participants:

The first two presenters in this symposium have diametrically opposed views of the prevalence and strength of adaptation in nature. Hendry believes that adaptation can be seen almost everywhere and that evidence for it is overwhelming and ubiquitous. Gonzalez believes that maladaptation is common and that there is ample theory and evidence for it. Neither author is certifiable to the knowledge of the other, leaving each to wonder where the other has his head buried. Extensive argument has revealed that each author thinks his own view is amply supported by both theory and empirical evidence. In our presentations, we each present devastating evidence supporting our own position and thus refuting that of the other. This juxtaposition sets the stage for the rest of the presentations, which will provide more level-headed and unbiased assessments of new evidence that bears on the ubiquity and (im)perfection of (mal)adaptation.

The first two presenters in this symposium have diametrically opposed views of the prevalence and strength of adaptation in nature. Hendry believes that adaptation can be seen almost everywhere and that evidence for it is overwhelming and ubiquitous. Gonzalez believes that maladaptation is common and that there is ample theory and evidence for it. Neither author is certifiable to the knowledge of the other, leaving each to wonder where the other has his head buried. Extensive argument has revealed that each author thinks his own view is amply supported by both theory and empirical evidence. In our presentations, we each present devastating evidence supporting our own position and thus refuting that of the other. This juxtaposition sets the stage for the rest of the presentations, which will provide more level-headed and unbiased assessments of new evidence that bears on the ubiquity and (im)perfection of (mal)adaptation.

Populations confronted to a changing environment, as occurs under climate change, must adapt fast enough to persist. Several theoretical models have formalized such demographic and evolutionary challenges and predicted the critical speed of environmental change, or the critical amount of genetic variance, above or below which, respectively, the population is doomed. Many species confronted to climate change have complex life cycles, with individuals in different stages differing in their ecology, their sensitivity to a changing climate and their contribution to population growth. Building on theoretical tools from evolutionary demography, we used a quantitative genetics model to predict the dynamics of adaptation in a stage-structured population confronted to a steadily changing environment. Our model assumes that the same phenotypic trait affects different transitions in the life cycle, with different optimal phenotypic values maximizing different fitness components, which generates de facto a trade-off between life history traits. In a constant environment, the population evolves towards an equilibrium trait value, which represents the best compromise given the trade-off between life history traits. In a changing environment however, the mean phenotype in the population will lag behind this optimal compromise. We show that this adaptive lag may result in a shift along the trade-off between life history traits, with negative consequences for some fitness components, but, less intuitively, improvements in some others. These shifts in life history could easily be wrongly interpreted as adaptations to the new environment, while they only reflect the inability of the population to adapt fast enough and are associated with lower fitness. More generally, we show how the critical speed of environmental change depends on its specific effects on different components of the life cycle.

Butterflies increase fitness by host-shifting to plants to which they are maladapted

Michael C. Singer, Plymouth University

The conference defines maladaptation as "evolution of relative and absolute fitness declines." However, maladaptation is a state of being as well as an evolutionary process and as such it can be associated with fitness increases. I will show that individuals adapted to a demanding environment increased fitness by shifting to a benign environment despite lacking traits that would adapt them to their novel lifestyle. I describe two independent episodes of evolution in which host-shifting Edith's checkerspot butterflies experienced higher fitness on novel hosts than on traditional hosts to which they were adapted.

In the first case, on a Nevada cattle-ranch, the traditional host was an ephemeral native Collinsia and the novel host a long-lived exotic Plantago. Despite slower development on Plantago, survival was higher and the insects rapidly evolved monophagy on it. Later, cattle were withdrawn, Plantagos were cooled by embedding in lush vegetation, and the butterfly population became extinct.

In the second case, the butterflies host-shifted from one native host, Pedicularis, to another, Collinsia. They were maladapted to the novel host in a complex suite of host-associated traits including visual search image, clutch size, geotaxis, preference for host phenology and larval performance. This maladaptation was experimentally confirmed by comparing performance in the field of local insects on both hosts with that of conspecifics transplanted from a population adapted to Collinsia. Fitness of the local Pedicularis-adapted insects was higher on Collinsia than on Pedicularis, but fitness on Collinsia of the imported Collinsia-adapted insects was highest of all.

The Galápagos Islands are renowned for their unique, endemic biodiversity which inspired Charles Darwin to develop his theory of evolution by natural selection. In particular, Darwin’s finches are an iconic example of adaptive radiation due to natural selection, where ~18 species have evolved from a single, common ancestor. Adaptive radiations can occur when speciation allows for the exploitation of new ecological niches. Darwin’s finches are illustrative of this with each species able to specialize on niche specific food items as well as through innovations such as tool use. Therefore each species of Darwin's finch is hypothetically happily perched on top of their appropriate fitness peak. However, humans can pose major threats to such adaptive radiations by altering adaptive fitness peaks, and thus, evolution. On the Galápagos Islands, humans have direct and indirect effects on the (mal)adaptation of Darwin's finches. Here, I focus on two human influences, introduced predators and introduced foods, and how Darwin's finches are (mal)adapting to humans on the Galápagos Islands.

The “Anna Karenina Principle”, which gets its name from Leo Tolstoy’s great tragedy of the same name, states that many steps are needed to achieve a goal and that deficiency at any one step dooms the entire endeavor to failure. Adaptive evolution is one such many-step process, so the Karenina Principle suggests that adaptation will rarely be completely successful. To introduce this symposium, in my talk I will summarize various ways of defining and measuring maladaptation, in both absolute and relative senses. These definitions help us enumerate a variety of reasons why adaptation may fail. Adaptation fails when populations are displaced from their local optimum by a change in the population mean (e.g., due to drift or gene flow), or by a change in the optimum (environmental change). Genetic variance is needed for natural selection to reduce such displacement and recover adaptation, but once the population mean reaches the optimum this same variance becomes genetic load. These familiar hurdles (and some less familiar ones) mean that we should reasonably expect that most populations are maladapted in some sense. To close, I present an analytical approach that quantifies symmetric or asymmetric local (mal)adaptation and outline how this analysis can help us test features of the Ana Karenina Principle.

Reciprocal transplant studies have provided many compelling examples of local adaptation, an important dimension of biodiversity. The ubiquity of local adaptation suggests that divergent natural selection usually overwhelms the potentially homogenizing effects of gene flow among populations and the random effects of genetic drift. However, local adaptation is not universal, and we lack a clear understanding of which factors actually create maladaptation in natural populations. We evaluate support for two, non-mutually exclusive hypotheses for maladaptation. The first hypothesis is that maladaptation increases towards range edges because edge populations are more prone to genetic drift or swamping gene flow. The second hypothesis is that maladaptation has increased in recent years because of rapid climate change, causing populations to no longer reside in the environments to which they are historically adapted. The first hypothesis predicts that maladaptation should increase with distance from the species’ geographic range centre, while the second hypothesis predicts that maladaptation increases with climatic anomalies and through time. We test these predictions through a quantitative analysis of 149 reciprocal transplant experiments that have measured the degree of local (mal)adaptation across broad spatial scales. We find that warm anomalies overturn the fitness advantage of local populations and instead favor warm-adapted foreign populations, supporting the hypothesis that climate change is causing maladaptation of natural populations.

Species’ ranges generally are thought to depend on constraints on adaptation to marginal habitats. This theory usually excludes biotic interactions entirely or focuses on competition. Predators, however, might often face environmental gradients that vary dynamically because their prey can adapt defenses against them. Here we develop theory about how the interplay between predator density and prey maladaptation generate divergent expectations about predator range limits, the distribution of abundances within ranges, and how predators respond to changing abiotic gradients. Given an underlying abiotic fitness gradient, predators become rarer toward their range edge. Assuming that prey defense trades off against other aspects of fitness, prey become more maladapted to predation risk as their predators become rarer, and gene flow swamps prey local adaptation. The predator meanwhile gains an energetic subsidy in the form of easily captured prey, which can facilitate its survival in marginal habitats and even aid its further expansion. Once the predator expands, the prey adapt to it, so the advantage disappears, creating an eco-evolutionary range boundary. Results provide insights about the determinants of species’ ranges as well as for more applied questions about range dynamics during environmental change.

The role of gene flow in causing or preventing maladaptation continues to be debated. Gene flow is classically viewed as a constraint to adaptive evolution by preventing selection from establishing and maintaining local genetic differences. But, gene flow can also reduce maladaptation through masking recessive deleterious alleles, heterozygote advantage, introducing novel high fitness alleles, or by increasing additive genetic variation on which selection can act. Fitness benefits of gene flow may be particularly important for contemporary populations that are fragmented and experiencing novel stress. However, it has never been directly shown that gene flow can prevent populations from extinction. I will present results from recent field and mesocosm experiments using Trinidadian guppies that shed light on conditions where gene flow is immediately beneficial, but also show the potential for long-term effects, including the prevention of extinction.

Human activities can drive rapid evolutionary responses in wild animal populations. These evolutionary responses often leave the population better able to cope with human activities, but sometimes populations appear to be maladapted to local conditions. Our ability to investigate the dynamics of these adaptive and maladaptive responses over time is typically limited in natural systems. I combined resurrection ecology and paleolimnology approaches to examine evolutionary responses of the freshwater zooplankter Daphnia to exposure to heavy metal contamination over the past 50-75 years using animals hatched from diapausing egg banks. In contrast to the predicted trend of adaptation to metal exposure over time, I found that Daphnia from contaminated time periods were more sensitive to copper and cadmium exposure. Given that the release of toxicants such as heavy metals is widespread and other researchers have observed local maladaptation to toxicant exposure, it is important to understand the drivers and implications of this pattern.

Evolutionarily-informed approaches in conservation typically focus on fostering adaptive responses to human modified environments. Goals guiding such approaches are generally aimed either at maintaining optimal traits (i.e. conservation for an adaptive state) or increasing adaptive potential (i.e. conservation for an adaptive process). When viewed through a traditional adaptive conservation framework, these two approaches are somewhat polar. The former aims to maximize current population fitness by reducing phenotype-environment mismatch. The latter, however, aims to maintain phenotypic variance to support adaptive responses in the future. Yet this variance should cause genetic load, increasing population maladaptation until adaptive outcomes are realized. Here, we attempt to bridge these seemingly conflicting goals through a (mal)adaptive view of conservation. We use meta-analysis to evaluate the advantages and disadvantages of these two different conservation strategies. We explicitly consider natural processes (e.g. migration load, introgression) and intervention tactics (e.g. hybridization, assisted migration) that can result in increased maladaptation but potentially lead to more sustainable populations. We highlight the ways in which a (mal)adaptive conservation framework can contribute to improved conservation management. In particular, management decisions made to support the process of adaptation must adequately account for maladaptation as an inevitable outcome and even as a tool to bolster adaptive capacity to changing conditions.